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SUSTAINING GLOBAL SURVEILLANCE AND RESPONSE TO EMERGING ZOONOTIC DISEASES Gerald T. Keusch, Marguerite Pappaioanou, Mila C. González, Kimberly A. Scott, and Peggy Tsai, Editors Committee on Achieving Sustainable Global Capacity for Surveillance and Response to Emerging Diseases of Zoonotic Origin Board on Global Health Institute of Medicine Board on Agriculture and Natural Resources Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This study was supported by the U.S. Agency for International Development Award No. GHN- G-00-07-00001-00. Any opinions, findings, conclusions, or recommendations in this docu- ment are those of the authors and do not necessarily reflect the views of the organizations or agencies that provided support for the project. Mention of trade names, commercial products, or organizations does not constitute their endorsement by the sponsoring agency. Library of Congress Cataloging-in-Publication Data Institute of Medicine and National Research Council (U.S.). Committee on Achieving Sustainable Global Capacity for Surveillance and Response to Emerging Diseases of Zoonotic Origin. Sustaining global surveillance and response to emerging zoonotic diseases / editors, Gerald T. Keusch ... [et al.] ; Committee on Achieving Sustainable Global Capacity for Surveillance and Response to Emerging Diseases of Zoonotic Origin, Board on Global Health, Institute of Medicine, Board on Agriculture and Natural Resources, Division on Earth and Life Studies. p. ; cm. Includes bibliographical references. ISBN 978-0-309-13734-8 (pbk.) 1. Zoonoses. 2. Public health surveillance. 3. Global health. I. Keusch, Gerald. II. Title. [DNLM: 1. Communicable Diseases, Emerging—prevention & control. 2. Zoonoses— epidemiology. 3. Biosurveillance—methods. 4. Disease Outbreaks—prevention & control. WA 110 I585s 2009] RA639.I57 2009 362.196’959--dc22 2009044034 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, NW, Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. For more information about the Institute of Medicine, visit the IOM homepage at: www. iom.edu. Copyright 2009 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Front cover, from top: Angus cattle on pasture. Photo by Scott Bauer, courtesy of USDA. Laboratory technician with diagnostic materials at the Washington Animal Disease Diagnos- tic Laboratory. Photo by Charlie Powell. Designation of H1N1 isolate digitally inserted by Photoshop. Researcher administers a new medication for bird flu to a young chicken. Photo by Steve Snowden, courtesy of iStockphoto. Laboratory scientist analyzes data at the Washington Animal Disease Diagnostic Laboratory. Photo by Henry Moore. Back cover, from top: Fruit bat surveillance. Photo courtesy of Wildlife Trust. A young male with a puppy on Independence Day in India. Photo by Jay Graham, courtesy of Photoshare. Deer runs through a suburban neighborhood. Photo by Lillis Photography, courtesy of iStockphoto. A girl carries two lambs in rural Bolivia. Photo by Enriqueta Valdez-Curiel, courtesy of Photoshare. Suggested citation: IOM (Institute of Medicine) and NRC (National Research Council). 2009. Sustaining global surveillance and response to emerging zoonotic diseases. Washington, DC: The National Academies Press.

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“Knowing is not enough; we must apply. Willing is not enough; we must do.” — Goethe Advising the Nation. Improving Health.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Acad- emy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding en- gineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineer- ing programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is presi- dent of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Insti- tute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sci- ences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Coun- cil is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON ACHIEVING SUSTAINABLE GLOBAL CAPACITY FOR SURVEILLANCE AND RESPONSE TO EMERGING DISEASES OF ZOONOTIC ORIGIN GERALD T. KEUSCH (Co-Chair), Boston University, MA MARGUERITE PAPPAIOANOU (Co-Chair), Association of American Veterinary Medical Colleges, Washington, DC CORRIE BROWN, University of Georgia, Athens JOHN S. BROWNSTEIN, Harvard Medical School, Boston, MA PETER DASZAK, Wildlife Trust, New York CORNELIS de HAAN, The World Bank (retired), Washington, DC CHRISTL A. DONNELLY, Imperial College London, United Kingdom DAVID P. FIDLER, Indiana University, Bloomington KENNETH H. HILL, Harvard University, Cambridge, MA ANN MARIE KIMBALL, University of Washington, Seattle RAMANAN LAXMINARAYAN, Resources for the Future, Washington, DC TERRY F. McELWAIN, Washington State University, Pullman MARK NICHTER, University of Arizona, Tucson MO SALMAN, Colorado State University, Fort Collins OYEWALE TOMORI, Redeemer’s University, Ogun State, Nigeria KEVIN D. WALKER, Michigan State University, East Lansing MARK WOOLHOUSE, University of Edinburgh, United Kingdom Study Staff KIMBERLY A. SCOTT, Study Director PEGGY TSAI, Program Officer MILA C. GONZÁLEZ, Research Associate SARAH JANE BROWN, Senior Program Assistant JULIE WILTSHIRE, Financial Officer PATRICK W. KELLEY, Director, Board on Global Health ROBIN A. SCHOEN, Director, Board on Agriculture and Natural Resources v

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BOARD ON GLOBAL HEALTH1 RICHARD GUERRANT (Chair), University of Virginia School of Medicine, Charlottesville JO IVEY BOUFFORD, New York Academy of Medicine, New York CLAIRE V. BROOME, Emory University, Atlanta, GA JACQUELYN C. CAMPBELL, Johns Hopkins University, Baltimore, MD THOMAS J. COATES, University of California, Los Angeles VALENTIN FUSTER, Mount Sinai School of Medicine, New York SUE GOLDIE, Harvard University, Boston, MA PETER J. HOTEZ, George Washington University, Washington, DC GERALD KEUSCH, Boston University, MA MICHAEL MERSON, Duke University, Durham, NC FITZHUGH MULLAN, George Washington University, Washington, DC PHILLIP RUSSELL, Johns Hopkins University, Baltimore, MD 1 IOM boards do not review or approve individual reports and are not asked to endorse conclusions and recommendations. The responsibility for the content of the report rests with the authoring committee and the institution. vi

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BOARD ON AGRICULTURE AND NATURAL RESOURCES NORMAN R. SCOTT (Chair), Cornell University, Ithaca, NY PEGGY F. BARLETT, Emory University, Atlanta, GA ROGER N. BEACHY, Donald Danforth Plant Science Center, St. Louis, MO HAROLD L. BERGMAN, University of Wyoming, Laramie RICHARD A. DIXON, Samuel Roberts Noble Foundation, Ardmore, OK DANIEL M. DOOLEY, University of California, Oakland JOAN H. EISEMANN, North Carolina State University, Raleigh GARY F. HARTNELL, Monsanto Company, St. Louis, MO GENE HUGOSON, Minnesota Department of Agriculture, St. Paul KIRK C. KLASING, University of California, Davis VICTOR L. LECHTENBERG, Purdue University, West Lafayette, IN PHILIP E. NELSON, Purdue University, West Lafayette, IN ROBERT PAARLBERG, Wellesley College, Watertown, MA KEITH PITTS, Marrone Bio Innovations, Davis, CA CHARLES W. RICE, Kansas State University, Manhattan HAL SALWASSER, Oregon State University, Corvallis PEDRO A. SANCHEZ, The Earth Institute, Columbia University, Palisades, NY ROGER A. SEDJO, Resources for the Future, Washington, DC KATHLEEN SEGERSON, University of Connecticut, Storrs MERCEDES VÁZQUEZ-AÑÓN, Novus International, Inc., St. Charles, MO vii

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Acknowledgments This report has been reviewed in draft form by persons chosen for their diverse perspectives and technical expertise in accordance with procedures approved by the National Research Council’s Report Review Committee. The purpose of the independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards of objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following for their review of this report: Sir George Alleyne, Pan American Health Organization Scott Barrett, Paul H. Nitze School of Advanced International Stud- ies, Johns Hopkins University Ron Brookmeyer, Johns Hopkins Bloomberg School of Public Health Donald S. Burke, Graduate School of Public Health, University of Pittsburgh Seth Foldy, Division of Public Health, State of Wisconsin Lawrence O. Gostin, Georgetown University David Harlan, Global Animal Health and Food Safety, Cargill, Inc. James M. Hughes, School of Medicine and Rollins School of Public Health, Emory University Anni McLeod, Food and Agriculture Organization of the United Nations Melinda Moore, RAND Corporation ix

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x ACKNOWLEDGMENTS Mark E. White, Division of Global Preparedness and Program Coor- dination, Centers for Disease Control and Prevention Tilahun Yilma, International Laboratory of Molecular Biology for Tropical Disease Agents, University of California, Davis Although the reviewers listed above have provided constructive com- ments and suggestions, they were not asked to endorse the conclusions or recommendations, nor did they see the final draft of the report before its release. The review of this report was overseen by David Challoner, Vice President for Health Affairs, Emeritus, University of Florida and James Fox, Massachusetts Institute of Technology. Appointed by the National Research Council and Institute of Medicine, they were responsible for making certain that an independent examination of this report was carried out in accor- dance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the author committee and the institutions.

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Preface In April 2009, as the committee was preparing to respond to reviewer input and finalize this report, a multi-country outbreak of a new influenza A(H1N1) virus was being reported. First detected as a cluster of cases of severe respiratory illness with multiple deaths in Mexico, a unique influenza A virus was isolated that was originally reported as having genes of swine, avian, and human origin and therefore it was immediately referred to as “swine flu.” Influenza A(H1N1) virus has since spread to 74 countries and, as of June 11, 2009, the World Health Organization declared it the first pandemic in more than 40 years. Although the virus is now circulating in humans, the presumed link with swine led to public confusion on how the virus was being spread, consequently leading to pork industry losses of approximately $28 million dollars per week and the banned importation of pigs and pork products by at least 15 countries. The specifics of when and how this virus emerged, in what populations, how long its circulation has gone undetected, and the identity of the source of exposure remain the focus of ongoing investigations. While it is not possible to fully analyze the progression and impact of events with the benefit of time and hindsight before completing the work on this report, this outbreak serves to illustrate many of the issues discussed in this report. The committee’s consensus report traces the need and existing capacity for global, sustained, integrated zoonotic disease surveillance and response capacity; discusses the current gaps, challenges, and inadequacies with ex- isting systems; and suggests new approaches to more effectively achieve the requirements of an “ideal” system. Looking forward with the benefit of past experience, including what we know about the current influenza A(H1N1) xi

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xvi CONTENTS The Human–Animal–Environment Interface, 78 Drivers Influencing Emerging and Reemerging Zoonoses, 83 Environmental Factors, 97 Technological Changes Leading to Emerging Disease, 101 Inadequate Governance, 106 Conclusion, 107 References, 107 4 ACHIEVING AN EFFECTIVE ZOONOTIC DISEASE SURVEILLANCE SYSTEM 115 Defining Disease Surveillance, 116 Elements of an Effective Zoonotic Disease Surveillance System, 117 Executing an Effective Zoonotic Disease Surveillance System, 119 Review of Existing Disease Surveillance Systems for Zoonotic Diseases, 129 Capacity-Building Programs to Create a Multidisciplinary, Integrated Workforce, 135 Gaps and Challenges, 138 Conclusion, 157 References, 157 5 INCENTIVES FOR DISEASE SURVEILLANCE, REPORTING, AND RESPONSE 165 Behavioral and Cultural Determinants of Information Sharing, 166 Economic and Trade Sanctions, 175 Incentives to Improve Disease Surveillance and Reporting, 178 Audit and Rating Framework for Disease Surveillance and Response Systems, 180 Engaging Multi-Level Stakeholders for Timely Disease Detection and Reporting, 181 Conclusion, 183 References, 184 6 SUSTAINABLE FINANCING FOR GLOBAL DISEASE SURVEILLANCE AND RESPONSE 187 Funding Animal Disease Surveillance, 187 Current Funding Efforts, 191 Funding a Global Public Good, 196 Funding Mechanisms, 197 The Institutional Architecture, 202 References, 203

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xvii CONTENTS 7 GOVERNANCE CHALLENGES FOR ZOONOTIC DISEASE SURVEILLANCE, REPORTING, AND RESPONSE 205 The Relationship Between Human and Animal Health Capabilities and Governance, 206 Governance Problems Facing Integrated Surveillance and Response Systems for Emerging Zoonotic Diseases, 211 Governance Innovations Supporting Integrated Disease Surveillance and Response in Human and Animal Health, 215 Moving Toward a Global, Integrated Disease Surveillance and Response System: Future Governance Strategies, 226 Conclusion, 232 References, 233 8 RECOMMENDATIONS, CHALLENGES, AND LOOKING TO THE FUTURE 235 Recommendations, 236 Challenges to Successfully Integrating and Coordinating International Disease Surveillance and Response Systems, 257 Looking to the Future, 263 References, 266 APPENDIXES A Glossary of Terms 269 B Surveillance and Response of Select Zoonotic Disease Outbreaks 277 C Novel Human Pathogen Species 293 D Public Committee Meeting Agendas 295 E Committee Biosketches 303

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List of Tables, Figures, and Boxes TABLES S-1 Recommendations by Priority and Category, 5 2-1 Selected Examples of Recent Zoonotic Outbreaks of International Significance, 38 2-2 Examples of Human Pathogens with Evolutionary Origins in Nonhuman Hosts, 52 4-1 Comparison of Disease Detection and Response Evaluation Standards for Human and Animal Health: International Health Regulations Versus Performance of Veterinary Services Tool, 130 4-2 Gaps and Challenges in Achieving an Effective, Global, Integrated Surveillance System for Emerging Zoonotic Diseases, 140 5-1 Policies That Influence Reporting at Various Levels, Who Is Affected, and Pros and Cons of Each Policy, 172 6-1 Avian and Human Influenza Pledges, Commitments, and Disbursements as of April 30, 2008, 193 6-2 Estimated Cost of Funding the One World One Health Framework to 2020, 195 6-3 Disease Prevention and Control Activities at the Human–Animal– Ecosystems Interface and Their Status Level as a Public Good, 197 xviii

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xix LIST OF TABLES, FIGURES, AND BOXES 6-4 Value of Meat Export by Country Income Category Group, 200 7-1 A Typology of Governance, 207 7-2 Substantiated Events by Initial Source of Official Information, 220 7-3 Events and Final Designation and Year of Reporting, 220 7-4 OIE Verification Requests and Responses to Them, 221 8-1 Recommendations for Improved Zoonotic Surveillance and Response by Priority and Category Areas, 237 C-1 List of 87 Novel Human Pathogen Species Discovered Since 1980, 293 FIGURES S-1 Zoonotic disease hotspots and selected reference laboratories by location, 10 1-1 Emerging infectious disease events detected from 1940 to 2004, 18 2-1 Total trade versus total agricultural trade, 29 2-2 International agricultural trade by commodity type, 1961–2006, 31 2-3 Trends in poultry production, 32 2-4 Number of confirmed human cases and deaths of avian influenza A (H5N1) reported to the World Health Organization by country and year, 37 2-5 Tourist arrivals in China and Thailand between 2001–2006, 43 2-6 Economic impact of a potential human influenza pandemic by percentage of GDP, 45 2-7 Household income and expenditure effects of a backyard poultry ban, 46 2-8 Opportunities to prevent, detect, and respond to the emergence and transmission of zoonotic diseases, 48 2-9 Patterns of pathogen discovery, 56 2-10 Patterns of reporting of emerging disease “events”: five countries reporting the highest number of “events” and selected others, 55 3-1 Overview of the driver-pathogen interactions that contribute to the emergence of infectious zoonotic diseases, 79 3-2 Projected production of animal meat by species, 1961–2025, 81 3-3 World population projections, median variant forecasts, 83

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xx LIST OF TABLES, FIGURES, AND BOXES 3-4 Volume of global air traffic, 1985–2001, and projection of future trends, 2001–2021, 85 3-5 Distribution of poultry in East and Southeast Asia, 93 3-6 Global swine distribution, 94 4-1 The cycle of elements comprising an effective infectious disease surveillance system, 117 4-2 System requirements for comprehensive human and animal health surveillance, 118 4-3 Zoonotic disease hotspots and selected reference laboratories by location, 152 4-4 Global World Health Organization Vaccine Preventable Disease Laboratory Network, 155 B-1 National and international response to the SARS outbreak, 282 BOXES 1-1 Statement of Task, 20 1-2 International Institutions and Actors, 23 2-1 Examples of the Underestimated Burden of Zoonotic Diseases, 41 2-2 The Economic Impact of Bovine Spongiform Encephalopathy Outbreaks in the United Kingdom, the United States, and Canada, 44 2-3 Selected Examples of the Balance and Imbalance Between Disease Surveillance and Emergency Response for Past Outbreaks, 50 2-4 Simulation of Human Influenza Transmission in Thailand, 60 2-5 Predicting an Outbreak, 62 3-1 Epidemiological Factors Comparing Natural and Man-made Ecosystems, 82 3-2 Advantages and Disadvantages of Intensive Agriculture Related to Zoonotic Diseases, 103 4-1 Definitions of Surveillance, 116 4-2 Summary of Data Types and Sources for Human and Animal Health Disease Events, 120 4-3 Prototypes of Web-Based Data Sources for Surveillance: ProMED-mail and GPHIN, 122 4-4 Principles of Good Laboratory Practice and Network Operation, 124

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xxi LIST OF TABLES, FIGURES, AND BOXES 4-5 ArboNET: Example of an Integrated Zoonotic Disease Surveillance System, 133 5-1 Nipah Virus Outbreak in Malaysia, 167 5-2 Definition of a Sanitary and Phytosanitary Measure at a Glance, 176 5-3 International Sanctions After a Plague Outbreak in India, 177 5-4 Making Vaccines Available to Incentivize Disease Reporting, 178 5-5 Google.org Predict and Prevent Initiative, 182 8-1 Model of an Integrated National Program for Zoonoses, 240 8-2 Philanthropic Support for Information Technology Development and Management, 244

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Acronyms and Abbreviations AHI Facility Avian and Human Influenza Facility APHIS Animal and Plant Health Inspection Service of the U.S. Department of Agriculture BSE bovine spongiform encephalopathy BSL biosafety level CAFO concentrated animal feeding operation CDC U.S. Centers for Disease Control and Prevention CITES Convention on International Trade in Endangered Species of Wild Fauna and Flora Codex WHO/FAO Codex Alimentarius Commission DHS U.S. Department of Homeland Security DoD U.S. Department of Defense DoD-GEIS U.S. Department of Defense-Global Emerging Infections Surveillance and Response System DoI U.S. Department of the Interior DoS U.S. Department of State ENSO El Niño-Southern Oscillation EU European Union FAO Food and Agriculture Organization of the United Nations xxiii

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xxiv ACRONYMS AND ABBREVIATIONS FDA U.S. Food and Drug Administration FELTP Field Epidemiology and Laboratory Training Program FETP Field Epidemiology Training Program FMD foot-and-mouth disease GAINS Global Avian Influenza Network for Surveillance GATT General Agreement on Tariffs and Trade of the WTO GDP gross domestic product GLEWS Global Early Warning System GOARN Global Outbreak Alert and Response Network GPAI Global Program for Avian Influenza GPHIN Global Public Health Intelligence Network HHS U.S. Department of Health and Human Services HLSC House of Lords Select Committee HPAI H5N1 highly pathogenic avian influenza H5N1 IDSR Integrated Disease Surveillance and Response IFI International Finance Institution IGO intergovernmental organization IHR 1969 International Health Regulations 1969 IHR 2005 International Health Regulations 2005 INCLEN International Clinical Epidemiology Network IOM Institute of Medicine IPCC Intergovernmental Panel on Climate Change IT information technology KEMRI Kenya Medical Research Institute NAHLN U.S. National Animal Health Laboratory Network NGO nongovernmental organization NRC National Research Council OIE Office International des Epizooties, also World Organization for Animal Health PCR polymerase chain reaction PEPFAR President’s Emergency Plan for AIDS Relief PHS Public Health Service Act ProMED Program for Monitoring Emerging Diseases PVS Performance of Veterinary Services tool RVF Rift Valley fever

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xxv ACRONYMS AND ABBREVIATIONS SARS severe acute respiratory syndrome SPS Agreement Agreement on the Application of Sanitary and Phytosanitary Measures SSAFE Safe Supply of Affordable Food Everywhere TBT Agreement Agreement on Technical Barriers to Trade UN United Nations UNSIC United Nations System Influenza Coordinator USAID U.S. Agency for International Development USDA U.S. Department of Agriculture USFWS U.S. Fish and Wildlife Service USGS U.S. Geological Survey vCJD variant Creutzfeldt-Jakob disease WAHIS World Animal Health Information System WHO World Health Organization WHO-AFRO World Health Organization Regional Office for Africa WNV West Nile virus WTO World Trade Organization

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